Immune challenge of female great tits at nests affects provisioning and body conditions of their offspring

The trade-off between animal’s parental reproductive effort and survival is still poorly understood. Parental allocation between the workload during breeding attempts and the parents’ own body conditions can be assessed through the offspring quality. Here, I questioned whether the immune responsiveness of female great tits may be considered as a mediator of this trade-off. Specifically, I tested whether (1) the parental reproductive effort decreases, (2) the food composition provided to chicks changes, and (3) whether the nestling immunocompetence and body mass decrease after experimental immunisation. Two populations of great tit Parus major occupying nest boxes were studied in Niepo?omice Forest and Krzyszkowice Forest (Southern Poland) in 2011 and 2012, respectively. Three days after hatching, half of the females were challenged with sheep red blood cells (SRBC), while other females were injected with phosphate-buffered saline PBS (control). Six days later, food provided by the parents was collected from nestlings. After another 2 days, the offspring’s body mass was measured and wing web swelling in response to an additional phytohaemagglutinin (PHA) injection. In both years, immunocompetence and in 2012 also body mass in the offspring of SRBC-immunised mothers were lower than in control nestlings, indicating a cost of mounting the immune response in the female. Six days after the start of the female treatment, the number of caterpillars and the volume of food items provided by parents to chicks were higher, whereas the number of spiders was lower in nests with SRBC treatment than in control ones. This might be explained by compensational parental feeding after recovery from the inflammation of a female. Thus, the trade-off between parental effort and survival of parents is mediated by the costs incurred for their immunity and can be assessed by the amount and quality of food provided to the nestlings and the offspring condition.     

The function of threat display in wintering great tits

It is generally accepted that threat displays have signal function and serve to repel opponents, but why they should have such an effect is a matter of debate. Using videotaped interactions from 2 years and nine flocks each year, we analysed the pattern of occurrence of agonistic displays and attacks in captive flocks of wintering great tits, Parus major. One currently influential perspective is to view threat interactions as sequences of distinct moves and countermoves, in which stronger threats can reliably indicate aggressive motivation because they carry a cost of eliciting counterattacks from certain opponents. We found little evidence for this kind of mechanism operating in great tits. Another possibility is that social dominance is important in ensuring reliable communication, for instance because an individual needs both to display and to attack to maintain its rank. It would be hard to test the importance of this kind of mechanism directly, but our observations were consistent with such an idea. Dominants won the majority of bouts of interaction and had higher rates of display and attack than subordinates, but a subordinate could temporarily overcome a dominant through intense aggression. We also found that the level of displaying in one bout provided information about the rate of aggression in following bouts. As a general interpretation of great tit aggressive behaviour, we suggest that particular displays form part of a graded signal of motivational state, so that a greater rate of displaying or a greater proportion of intense displays, together with a greater rate of attacking, correspond to a greater aggressive motivation. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Social environment affects juvenile dispersal in great tits (Parus major)

1.?Habitat selection can affect individual fitness, and therefore, individuals are expected to assess habitat quality of potential breeding sites before settlement. 2.?We investigated the role of social environment on juvenile dispersal behaviour in the great tit (Parus major). Two main contradictory hypotheses can be formulated regarding social effects on juvenile dispersal as follows: (i) High fledgling density and sex ratio may enhance the intensity of local (kin) competition and, therefore, reduce individual survival chance, enhance emigration and reduce settlement ('repulsion' hypothesis) (ii) Alternatively, high fledgling density and sex ratio may signal high-quality habitat or lead to aggregation and thus increase individual survival chance, reduce emigration and enhance settlement ('attraction' hypothesis). 3.?To disentangle positive from negative effects of high density and male-biased sex ratio on dispersal, we manipulated the social composition of the fledgling population in 12 semi-isolated nest-box areas (plots) via a change of fledgling density (low/high) as well as fledgling sex ratio (female-biased/balanced/male-biased) across 3?years. We then tested whether experimental variation in male and female fledgling densities affected variation in local survival, emigration and settlement of juveniles, and whether social effects on survival and dispersal support the 'repulsion' or 'attraction' hypothesis. 4.?We found no experimental effects on local survival and emigration probabilities. However, consistent with the 'attraction' hypothesis, settlement was significantly and positively affected by local experimental sex ratio in each of the study years: both male and female juveniles avoided female-biased plots and settled more in plots that were balanced and male-biased the previous year. 5.?Our study provides unprecedented experimental evidence that local sex ratio plays a causal role in habitat selection. We suggest that settlers avoid female-biased plots because a high proportion of females may reflect the absence or the low quality of local resources in the habitat. Alternatively, male territory acquisition may be facilitated by a high local density of 'candidate' males, and therefore, juveniles were less successful in settling in female-biased plots.     

Experimental removal of the male parent negatively affects growth and immunocompetence in nestling great tits

Given the available empirical evidence on the benefits and costs associated with immune defence, a role for the immune system in the trade-off between current and future reproduction has been predicted. This hypothesis was studied in a free-living population of great tits (Parus major) by examining the effects of male removal on the immunocompetence, body condition, and recapture probability in the widowed females and their nestlings. Furthermore, we investigated whether growth and its relation to immunocompetence were affected in the nestlings. For a short-lived species such as the great tit, one could predict that widowed females will compensate for the lack of any male assistance in feeding of their chicks and that they consequently might jeopardize their own health. However, we did not find any negative effects of male removal on body mass or condition, nor on humoral immunocompetence against sheep red blood cells in the widowed females by the end of the feeding period. In contrast, we observed significantly reduced body mass and size as well as a reduced T-lymphocyte cell-mediated immune response (expressed as the thickness of the swelling to a subcutaneous injection with phytohemagglutinin) in the experimental nestlings compared to the control nestlings. In addition, the experimental nestlings showed a tendency for a reduced chance to be found breeding the following year. Furthermore, our results showed that in the experimental nestlings, which suffered from unfavourable growth conditions, tarsus length was inversely related to cell-mediated immunocompetence, whereas in control nestlings this relationship was significantly positive. The relationship between cell-mediated immunity and body condition was found to be significantly positive in the experimental nestlings while in control nestlings there was no relationship between both variables. The latter finding suggests different priorities of investment in body condition between different growth conditions.     

Nocturnal loss of body reserves reveals high survival risk for subordinate great tits wintering at extremely low ambient temperatures

Winter acclimatization in birds is a complex of several strategies based on metabolic adjustment accompanied by long-term management of resources such as fattening. However, wintering birds often maintain fat reserves below their physiological capacity, suggesting a cost involved with excessive levels of reserves. We studied body reserves of roosting great tits in relation to their dominance status under two contrasting temperature regimes to see whether individuals are capable of optimizing their survival strategies under extreme environmental conditions. We predicted less pronounced loss of body mass and body condition and lower rates of overnight mortality in dominant great tits at both mild and extremely low ambient temperatures, when ambient temperature dropped down to ?43 °C. The results showed that dominant great tits consistently maintained lower reserve levels than subordinates regardless of ambient temperature. However, dominants responded to the rising risk of starvation under low temperatures by increasing their body reserves, whereas subdominant birds decreased reserve levels in harsh conditions. Yet, their losses of body mass and body reserves were always lower than in subordinate birds. None of the dominant great tits were found dead, while five young females and one adult female were found dead in nest boxes during cold spells when ambient temperatures dropped down to ?43 °C. The dead great tits lost up to 23.83 % of their evening body mass during cold nights while surviving individuals lost on average 12.78 % of their evening body mass. Our results show that fattening strategies of great tits reflect an adaptive role of winter fattening which is sensitive to changes in ambient temperatures and differs among individuals of different social ranks.     

Immune challenge affects sexual coloration of male Iberian wall lizards

Sexual signals can be evolutionarily stable if they are honest and condition dependent or costly to the signaler. One possible cost is the existence of a trade-off between maintaining the immune system and the elaboration of ornaments. We experimentally challenged the immune system of male Iberian wall lizards, Podarcis hispanica, with a bacterial antigen (lipopolysaccharide) without pathogenic effects to explore whether the immune activation affected sexually dimorphic visual ornaments. Ventrolateral coloration changed in all males, but immune activation affected some characteristics of coloration of experimental males (i.e., challenged males failed to increase brightness and medium wavelengths over time as control males did, and the proportion of yellow pigments decreased after the immune activation) but not others (i.e., proportion of blue, green and red pigments changed equally in all males). Results suggested the existence of a trade-off between physiological regulation of the immune system and the allocation of essential compounds (probably carotenoids) to sexual ornaments. We suggest that this trade-off may allow one to honestly signal individual male quality via characteristics of coloration in lizards, which may have an important role in both intra- and intersexual selection processes.     

Health impact of blood parasites in breeding great tits

Hypotheses of hemoparasite-mediated sexual selection and reproductive costs rely on the assumption that avian blood parasite infections are harmful to their hosts. To test the validity of this assumption, we examined the health impact of Haemoproteus blood parasites on their great tit (Parus major) host. We hypothesised that if blood parasites impose any serious health impact on their avian hosts, then infected individuals must differ from uninfected ones in respect to hemato-serological general health and immune parameters. A 3-year study of two great tit populations, breeding in contrasting (urban and rural) habitats in south-east Estonia, revealed that Haemoproteus blood parasites affected the health state of their avian hosts. Infected individuals had elevated lymphocyte hemoconcentration and plasma gamma-globulin levels, indicating that both cell-mediated and humoral immune response mechanisms are involved in host defence. The effect of parasites on cell-mediated immunity was both age- and sex-specific, as infection status affected peripheral blood lymphocyte counts only in males, and among these, the magnitude of response was greater in old individuals than yearlings. Heterophile hemoconcentration and plasma albumin levels were not affected by infection status, suggesting that blood stages of Haemoproteus infection do not cause a severe inflammatory response. Parasitism was not related to hematocrit values, indicating that Haemoproteus infection does not cause anemia. In two years, infected individuals were heavier than uninfected ones in the urban but not in the rural study area. This suggests, that under certain circumstances (possibly related to reproductive tactics), breeding great tits may avoid losing body mass in order to save resources for an anti-parasite immune response. Received: 16 February 1998 / Accepted: 22 May 1998     

Female genetic heterogeneity affects the reproduction of great tits (Parus major L., 1758) in low-quality woodlands

Genetic heterogeneity is considered an important parameter for individual fitness and reproductive success. In 1999 and 2000, we studied the population genetics of great tit ( Parus major L., 1758) in southwestern Germany from two different forest types (deciduous and mixed-coniferous), which may significantly differ in prey diversity and/or food supply. Adults of 99 families were genotyped at four enzyme and eight microsatellite loci, in order to estimate individual heterozygosity. In the mixed-coniferous forest, a significant positive correlation between the genetic heterogeneity of females and early egg-laying date and clutch size was detected. Early egg-laying date and increased clutch size are conditions that positively affect the number of fledglings. This effect of individual heterozygosity was not observed in the deciduous woodland. Maternal genetic heterogeneity, however, did not correlate with fledgling condition, and individual heterozygosity of fathers had no impact on breeding success in either habitat. The positive effect of female genetic heterogeneity on brood size of great tits in mixed-coniferous forests is attributed to early egg-laying date, i.e. a maternal effect, rather than to a specific mating strategy that optimizes fitness through an increased brood size and the quality of offspring.     

Clutch size and malarial parasites in female great tits

life-history models predict an evolutionary trade-off in theallocation of resources to current versus future reproduction.This corresponds, at the physiological level, to a trade-offin the allocation of resources to current reproduction or tothe immune system, which will enhance survival and thereforefuture reproduction. For clutch size, life-history models predicta positive correlation between current investment in eggs andthe subsequent parasite load. In a population of great tits,we analyzed the correlation between natural clutch size of femalesand the subsequent prevalence of Plasmodium spp., a potentiallyharmful blood parasite. Females that showed, 14 days after hatchingof the nestlings, an infection with Plasmodium had a significantlylarger clutch (9.3 eggs ± 0.5 SE, n = 18) than uninfectedfemales (8.0 eggs ± 0.2 SE, n = 80), as predicted bythe allocation trade-off. Clutch size was positively correlatedwith the prevalence of Plasmodium, but brood size 14 days afterhatching was not. This suggests that females incur higher costsduring laying the clutch than during rearing nestlings. Infectionstatus of some females changed between years, and these changeswere significantly correlated with a change in clutch size aspredicted by the trade-off. The link between reproductive effortand parasitism may represent a possible mechanism by which thecost of egg production is mediated into future survival andmay thereby be an important selective force in the shaping ofclutch size     

Alarm calls of wintering great tits Parus major: warning of mate,reciprocal altruism or a message to the predator?

When a predator is not an immediate threat, a prey may produce relatively loud alarm calls because the risk is low. Since such calls could nevertheless attract acoustically oriented predators, the cost of predator attraction must be outweighed by factors beneficial to the caller. In this field study we elicited low-risk alarm calls by temporarily catching wintering adult male great tits Parus major at feeders both within and outside their territories. We tested whether the alarm calls of dominant males can be explained in terms of mate warning, reciprocal altruism or notifying the predator of detection. If alarms are intended to warn mates, males accompanied by their mates should give alarm calls both within and outside home range, even if other permanent flock members are absent. If alarms are to be explained by reciprocal altruism, male great tits should give low-risk alarm calls when accompanied by permanent flock members other than mate within and not outside of the home-range. If alarm calling is a message to a predator, males should call when foraging alone. We found that male great tits gave low-risk alarm calls when accompanied by their mates, independent of feeder location. They also gave low-risk alarm calls within home ranges in the presence of other permanent flock members when mates were absent. In contrast, only a few males gave calls when foraging alone within their home ranges, or when in the company of unfamiliar great tits outside their usual home-range. The results suggest that the utterance of alarm calls may be explained as mate protection and reciprocal altruism among familiar individuals.     

Experimental evidence for density dependence of reproduction in great tits

1. Density dependence of avian reproduction has often been analysed using correlations between annual mean reproductive output and population density. Experiments are necessary to prove that density is the cause of the observed patterns, but so far, three out of four experimental studies do not support a direct causal effect of density on reproduction.
2. This paper presents experimental evidence that reproductive decisions in great tits, Parus major L., are causally affected by breeding density. The breeding density of great tits was manipulated by providing nest-boxes at different densities in an ecologically homogeneous area.
3. Within years the densities in the high and low density plots differed approximately 8-fold. During the 11 years of the experiment, clutch size, nestling mass and the proportion of birds starting a second brood were all lower in the high density plot. In 5 years with equal breeding densities in both parts, clutch size did not differ between the plots. The patterns found were consistent with the density effects as predicted from the non-experimental data.     

Social stability and daily body mass gain in great tits

This paper presents the results of an experiment on the influenceof changes in flock composition and social rank on the patternof daily mass gain in captive wintering great tits. We createdflocks of three male great tits and scored dominance when rankshad stabilized after a few days. We then moved the dominantbird from each flock into a neighboring flock, thus creatinga certain amount of social instability and unpredictable resourceaccess. Both before and after moving the dominants, we collectedindividual body mass data three times a day. When the hierarchieshad stabilized in the second flocks, individual ranks were scored.After the dominant birds were moved, the rate of daily massgain increased for the average individual. There was also adecrease in average morning body mass, so the birds startedthe day at a lower mass and ended at a slightly higher massthan previously. Dominants were on average heavier than subordinates,but we found no statistically significant effect of rank changeon body mass. The pattern of daily mass gain was linear overtime both before and after treatment. We conclude that an impressionof unpredictable resource access can be created by disturbingthe social structure in a flock, with similar effect as fromrestricting individual access to feeders. Within a flock, instabilityof the social hierarchy thus seems to have an influence on bodymass management in addition to that of environmental stochasticity.